Ticks and tick-borne pathogens along the routes of bird migration: the role of trans-Saharan migratory birds in introducing exotic ticks and emerging zoonotic agents in Italy

Climate and environmental changes, together with habitat modifications due to anthropogenic pressure, are rapidly causing changes in ecosystems and species distribution worldwide. Human and animal migratory movements contribute to the new scenario, favouring the dispersion of vector parasites originating in the tropical and subtropical regions of the globe and, consequently, of vector-borne pathogens which pose a threat to human and animal health worldwide. Ticks are among the most common parasites of vertebrates, and vectors of viral and bacterial diseases, and have an extremely wide range of distribution. Despite their limited ability in movement, they can be easily disseminated far from their original range thanks to their hosts, among which migratory birds have a prominent role due to their unique ability to fly long distances between continents in a short time and to cross geographical barriers. This study investigated the role of trans-Saharan migratory birds in the spread of ticks and tick-borne pathogens during the spring migration from Africa to Italy. The screening for ticks directly from migrating birds was conducted during the ringing activities within the “Small Islands Projects” at the bird-ringing station on the island of Ventotene, in the central Tyrrhenian Sea, one of the most important stop-over sites for migratory birds in Italy. The ticks were collected, subjected to morphological and molecular identification, and tested individually for the presence of Crimean-Congo haemorrhagic fever virus (CCHFV), Coxiella burnetii, and Rickettsia species. Data resulting from tick-host association and tick identification were then analysed to assess the effect of ecological and phenological traits of different species of migratory birds on tick infestation rate and, consequently, on the potential spread of these vectors from Africa to Italy. Preliminary analysis of infestation data of trans-Saharan migratory birds by African ticks conducted over three of the five years of collection indicated that feeding behaviour, size (body weight), migration phenology, and year significantly influence the probability of being infested, while no effect of habitat type or latitude of the wintering area was observed. The identification of the ticks highlighted the overall high prevalence (>70%) of African species within the collection, all of them known to be relevant biological vectors of tick-borne pathogens. The predominant species was Hyalomma rufipes, followed by a small but constant number of Amblyomma specimens belonging to the Amblyomma marmoreum complex, whose exact identification at the species level is still under discussion. Furthermore, the study pointed out the unusual presence of allochthonous soft ticks, such as Argas vulgaris, Ar. persicus, and a new genotype close to Ar. africolumbae, on migrating birds. During the screening for pathogens in ticks carried by migratory birds, CCHFV RNA was not found during the 2021-2022 survey, while the second report for Italy (2018) is presented in this thesis, confirming the role of migratory birds in the potential spread of the disease to Central Mediterranean countries. Results of screening for bacteria showed a high prevalence (>50%) of Rickettsia infection in ticks, mainly represented by R. aeschlimannii, found strictly associated with H. rufipes ticks, followed by other species extensively described in Italy, and by two possible new allochthonous species for Italy, namely, R. tamurae and R. asembonensis. Conversely, the suspected C. burnetii detected in two soft ticks were confirmed as Coxiella-like endosymbionts and not the pathogen. All the findings resulting from this thesis strongly support the active role of trans-Saharan migratory birds in the spread of ticks and tick-borne pathogens of human concern from Africa, and highlighthe need for continuous surveillance to monitor the potential emergence of new tick-borne diseases in Italy.